turner, a. , tisdall, d., barrett, d. c., wood, s., dowsey ...andrea turner, david tisdall, david c....
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Turner, A., Tisdall, D., Barrett, D. C., Wood, S., Dowsey, A., & Reyher, K.K. (2018). Ceasing the use of the highest priority critically importantantimicrobials does not adversely affect production, health or welfareparameters in dairy cows. Veterinary Record, 183(2), [67].https://doi.org/10.1136/vr.104702
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Ceasing the use of the highest priority critically important antimicrobials does not adversely affect
production, health or welfare parameters in dairy cows
Andrea Turner, David Tisdall, David C. Barrett, Sarah Wood, Andrew Dowsey, Kristen K. Reyher
Abstract
Due to scientific, public and political concern regarding antimicrobial resistance (AMR),
several EU countries have already taken steps to reduce antimicrobial (AM) usage in
production animal medicine, particularly that of the highest priority critically important AMs
(HP-CIAs). While veterinarians are aware of issues surrounding AMR, potential barriers to
change such as concerns of reduced animal health, welfare or production may inhibit progress
towards more responsible AM prescribing.
Farmers from seven dairy farms in South West England engaged in changing AM use
through an active process of education and herd health planning meetings. Prescribing data
was collected from veterinary sales records; production and health data were accessed via
milk recording and farm-recorded data.
This study demonstrates that cattle health and welfare - as measured by production
parameters, fertility, udder health and mobility data, and culling rates - can be maintained and
even improved alongside a complete cessation in the use of HP-CIAs as well as an overall
reduction of AM use on dairy farms.
This study also identified a need to consider different metrics when analysing AM use data,
including dose-based metrics as well as those of total quantities to allow better representation
of the direction and magnitude of changes in AM use.
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Introduction
Antimicrobial resistance (AMR) within production animal populations is of increasing
scientific, public and political concern. A recent review of published literature highlighted
that, for some bacteria, AMR patterns seen in humans could be a result of antimicrobial (AM)
use in livestock (1). There are also increasing reports of resistant bacteria being recovered
from production animals (2-5), that the use of certain classes of antibiotics in livestock
increase the risks of multiresistant bacteria being present on farms using these medicines (6,
7), and that decreasing the use of these classes of antimicrobials can reduce the prevalence of
resistance on these farms (8).
Fluoroquinolones and third and fourth generation cephalosporins have been identified as
‘highest priority critically important antimicrobials’ (HP-CIAs) for human medicine by
national and international bodies including the World Health Organisation (WHO), World
Organisation for Animal Health (OIE) and the Food and Agriculture Organisation of the
United Nations (FAO). Several EU countries have already taken steps to reduce AM use in
production animal medicine (9, 10) with recent focus on the reduction of HP-CIAs.
Prophylactic use of AMs is also under scrutiny as this practice has been demonstrated to
increase the prevalence of multidrug resistant bacteria (11). Veterinary surgeons (VSs) in the
UK have a crucial role to play in the reduction of AM administration on farms: although AMs
are commonly administered by farm staff (12, 13), prescription-only veterinary medicines
(POM-V), such as AMs, may only be used if prescribed by a VS, who is therefore ultimately
responsible for their use. Furthermore, as a trusted source of information to farmers (13), VSs
are well-placed both to implement changes in prescription practice and to educate and
motivate farmers and farm staff to engage with disease prevention strategies and more
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responsible AM use, all of which have been identified as ‘areas of action’ to reduce AMR
(14).
Whilst many VSs understand and appreciate concerns surrounding the use of AMs in
production animal medicine (15), there are also other influences on prescribing practice.
Practitioners often feel that they need to respond to farmer expectations of AM prescribing
(16, 17) and farmers, in turn, have concerns over potential reduced animal health, welfare and
production parameters, as well as financial issues associated with reducing or changing AM
use on their farms (13, 18). Despite these concerns, a majority of UK dairy farmers feel that
reducing AM use in their dairy herds would be beneficial and could reduce production costs,
and that their peers (other farmers and VSs) would think favourably of them doing so (13).
For VSs working in production animal medicine, the challenge of achieving more responsible
and sustainable AM use can offer an opportunity to advance dialogue with farmers about on-
farm treatment protocols, employing preventive rather than reactive management of animal
health and active herd health management.
The primary aim of the study was to investigate the effect of the cessation of use of HP-CIAs,
at farm level on associated animal health, welfare and production parameters. Other aims
were to describe the reduction in AM use using appropriate metrics and to delineate the
process by which prescribing practices were changed on the participating farms. The
hypothesis was that cessation of the use of HP-CIAs would not be associated with
deterioration of health, welfare or production on the dairy farms investigated. Throughout the
study HP-CIAs are defined according to guidelines from the European Medicines Agency, as
has been adopted by the Responsible Use of Medicines in Agriculture Alliance, namely third
and fourth generation cephalosporins, fluoroquinolones and colistin ( 20).
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Materials and methods
Data collected for this study originated from seven dairy farms, all of which were current
clients of the Langford Farm Animal Practice (FAP), North Somerset, UK. Data were
collected between 1st January 2010 and 31st December 2015.
Implementing prescribing changes
In 2010, VSs at the FAP began an initiative to reduce the use of HP-CIAs on all farms under
the care of the practice. During 2010-11 farmers were engaged and educated about this
process through farmer meetings and herd health planning visits; during 2011-12 changes to
prescribing policy and on-farm use were implemented on pilot farms (Farms 2 and 3).
Subsequently, changes were extended to all farms through the following years (2012-15),
including one farm that joined the practice at the end of 2013 (Farm 6) on which changes in
AM use were implemented from January 2014. Despite changes being implemented
sequentially across study farms, AM use data were available for all farms for the whole study
period. Farms worked closely with different VSs from the practice during this time, but the
same changes to prescribing practice were encouraged on all farms throughout this entire
process. It was deemed that all substantial changes had been made on all farms by the end of
2014, so at least one year of follow-up data were available for comparison across all farms.
On-farm treatment protocols were changed so that HP-CIAs were not kept on farms and were
only prescribed by VSs after examination of an animal. Gradually the use of HP-CIAs was
phased out entirely by both farmers and VSs for any empirical treatment decision. The most
significant changes were: 1) from early 2010 fluoroquinolones were no longer used or
prescribed by the practice; 2) fourth generation cephalosporins used in lactating cow
intramammary tubes were replaced with products containing penicillin and aminoglycoside
preparations; 3) third generation cephalosporins, widely used as injectable preparations, were
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replaced with first generation cephalosporins or aminopenicillins. Practice policy stated that
HP-CIAs were only to be considered if indicated by the results of culture and sensitivity
testing.
Strategies to encourage and improve animal management and husbandry were also
implemented alongside changes in AM use. These included, but were not limited to, the
increasing use of medicine audits and reviews to guide herd health planning and engage
farmers in changing and reducing AM use, farmer education including evening meetings and
practical classes, and increased herd health monitoring through clinical scoring (mobility
scores/ body condition scoring) and sampling (milk cultures, metabolic profiling etc).
Herd inclusion
Herds were included in this study if they milk recorded monthly and kept sufficiently detailed
fertility and disease incidence records to allow analysis of specific health parameters (see
Supplementary Materials).
Data collection
Health, fertility and milk recording data were captured in Interherd software (Pan Livestock
Services Ltd, Reading UK) or bespoke spreadsheets and then either extracted directly from
these or after further analysis in another software package (TotalVet, SUM-IT Computer
systems Ltd, Thame, UK; Figure 1). A full explanation of the data collection process and
definition of disease parameters are described in the Supplementary Materials.
Data for each health and welfare parameter were imported into the R programming
environment (R-prject.org), log-transformed so that regression results represented percentage
change per year, and then modelled by random-intercept regression using the Bayesian
MCMCglmm package (21). 130,000 MCMC samples were simulated with the first 30,000
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discarded as burn-in. For each health and welfare parameter, the slope of the fitted regression
curve as percentage change per year of the mean (M) and the Bayesian equivalent of
confidence intervals, the 95% credible interval (CI), are reported.
Antimicrobial prescribing
Data collection
Antimicrobial prescribing and sales data were accessed via practice management
software (RXWorks, Newbury, UK). From this software, a list of all AM sales to each of the
farms in the study was obtained for each of the study years (1st January – 31st December
2010-15), in addition to this AM sales data were provided by the veterinary practice
supplying medicines to Farm 6 in 2010 - 13. Sales data were entered into a spreadsheet
(Microsoft Excel, 2013) for analysis and total kilograms (kg) of AMs used per year as well as
Animal Daily Dose per animal per year (ADD), as defined by Dupont and colleagues (22),
were calculated. Further information regarding the calculation of the AM use metrics and AM
classification are included in the Supplementary Materials.
Results
Farm descriptions
All seven farms were located within a 20-mile radius of Langford FAP in South West
England. All farms reared their own heifer replacements, had all-year-round calving patterns
and, when housed, kept cows in cubicles (freestalls). All but two farms performed selective
dry cow therapy (SDCT) at the start of the study period (23) (see Supplementary Materials
for SDCT protocol). The farms practicing SDCT treated, on average, 36% of cows with AMs.
Mean percentage of cows dried off using AMs across all study farms across all years was
53%. Farm 6 began SDCT during 2014. Descriptive information regarding farm management
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and on-farm data recording are presented (Tables 1 and 2).
Antimicrobial prescription
In 2010, third and fourth generation cephalosporins were being prescribed to all seven farms
(Figure 2). None of the six FAP clients were prescribed any fluoroquinolones throughout the
study, meaning the reductions seen in HP-CIA use on these farms is solely due to reduced
prescriptions of 3rd and 4th generation cephalosporins. Notably, Farm 6 (which became a
client of the practice at the end of 2013) was being prescribed a similar amount of HP-CIAs
from 2010-13 when compared to farms that were clients of the FAP at this time (Figure 2).
Unlike the other farms, Farm 6 was prescribed small quantities of fluoroquinolones in 2011
(2.5 ADD) and 2013 (7 ADD). Colistin was not used on any farms throughout the study.
Due to the changes in prescribing practices, the total quantity of HP-CIAs reduced from 0.9
kg or 7.2 ADD in 2010 (accounting for 6.3% and 41.0% of kg and ADD, respectively) until
they were not prescribed to any farms in 2015. HP-CIA prescriptions consistently accounted
for a larger proportion of ADD than kg of AMs.
The majority of HP-CIAs prescribed in 2010 across the seven farms were licenced for
systemic administration (77% kg, 61% ADD; Table 3). Intramammary (lactating cow)
preparations containing 3rd and 4th generation cephalosporins also significantly contributed to
total quantities of HP-CIAs prescribed (23% kg, 39% ADD), although no dry cow
intramammary preparations containing HP-CIAs were prescribed throughout the six years of
the study. From 2010 to 2015, HP-CIA-containing intramammary tubes constituted 26, 24, 8,
3, 0 and 0% of all intramammary preparations, respectively, by kg and 57, 58, 21, 8, 0 and
0%, respectively, by ADD.
Overall, systemic AMs accounted for the largest quantities of AM prescriptions to each farm
(by both kg and ADD) followed by intramammary preparations. The use of intrauterine and
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topical AMs was low across all years (Table 3).
Both metrics show variation in the quantities of AMs being prescribed to the study farms
each year; both the total kg of AMs prescribed and the total number of ADD prescribed to the
study farms increased in 2012 and 2013 before reducing through 2014 and 2015. When
represented in ADD, AM prescription in 2015 was lower than in any previous year of the
study (16.7 ADD; Table 3).
The mean AM prescription across all study farms was also calculated in mg/kg for each year
of the study and was found to be 14.0, 12.0, 17.5, 18.0, 15.1 and 12.7 mg/kg respectively
between 2010 and 2015. The minimum value at the farm level was 5.0 mg/kg and the
maximum value was 35.3 mg/kg for individual farms across all years of the study.
The increase in the total quantity of AMs prescribed in 2012, as measured in both kg and
ADD, was largely due to an increase of penicillins (including penicillin in combination with
streptomycin), and 1st generation cephalosporins (Table 4). There was little change in the
prescription of anti-pneumonial AMs considered to be used primarily for the treatment of
calves (tetracyclines, chloramphenicol derivatives and macrolides, including long-acting
macrolides) over the six years of the study (2.2, 2.0, 1.7, 2.3, 2.1 and 1.8 kg, respectively,
through 2010-15), accounting for 0.1 ADD in 2010 and decreasing to 0.08 ADD in 2015.
Production parameters
Mean 305-day milk yield showed an increasing trend, with a mean increase of 0.6% per year
over the six years of the study (95% CI [-0.2, 1.4]; Figure 3).
Fertility parameters
Fertility parameters showed an improving trend over the course of the six-year study period.
Mean 100-day in-calf rate increased across the seven farms from 0.4 in 2010 to 0.5 in 2015
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(M 5.0%; 95% CI [1.8, 7.8]) (Figure 4A). Calving index decreased from 413 days in 2010 to
390 days in 2015 (M -0.9 %; 95% CI [-1.4, -0.5]); Figure 4B). During the same period, mean
calving to conception interval showed a decreasing trend from 147 days in 2010 to 120 days
in 2015 (M -2.8%/yr; 95% CI [-5.8, 0.2]). During the study period, the mean endometritis
failure to cure rate is unlikely to have changed (M -5.7%/yr; 95% CI [-19.5, 7.6]).
Udder health parameters
Clinical mastitis case rate (as recorded by farmers) decreased on five of the seven farms
between 2010 and 2015 (Figure 5A). On Farm 1, clinical mastitis cases rose from 10
cases/100 cows/year to 29 cases/100 cows/year. The on-farm records of clinical mastitis for
Farm 5 were not complete and so are not included in the analysis. From 2010-15, mean
mastitis cure rates (as measured by somatic cell counts, SCC) showed a mean increase of
7.5%/yr (95% CI [1.2, 13.3]; Figure 5B). Mean dry cow cure rates showed a decreasing trend
(M -1.3%; 95% CI [-2.9, 0.2]).
Subclinical mastitis risks, as assessed by mean proportion of cows with SCC over 200,000
cells/ml and the mean percentage of cows chronically infected (SCC>200k for two
consecutive milk recordings) are unlikely to have changed (M 1.0%; 95% CI [-2.2, 4.4] and
M 2.2%, 95% CI [-2.1, 6.9], respectively). Variation in the 12-month rolling bulk milk SCC
which ranged from 161 in 2013 to 262 in 2014 is largely due to extreme variability in the
bulk milk SCC on one farm (Farm 1; Figure 6).
Lameness
The percentage of cows scored as lame at mobility scoring sessions performed by VSs
decreased over the six years of the study on all farms with complete data (M-18.2%; 95%CI
[-25.5, -12.5]) (Figure 7).
Culling
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Culling percentages ranged from 13 to 33% across the seven farms in 2010 and remained
within this range throughout subsequent years of the study (M -3.7%; 95% CI [-7.9, 0.3];
Figure 8). While certain farms decreased the percentage of the herd culled each year (Farm
2), others increased the culling percentage overall (Farm 6), and there was variability both
within and between farms.
Discussion
The aims of this study were to describe how prescribing policy was changed to achieve a
cessation in HP-CIA use on seven dairy farms, to appropriately assess these AM use changes
using two different metrics and to examine the effects of discontinued HP-CIA use on cattle
health and welfare.
Farms were selected as a convenience sample due to inclusion criteria. It is accepted that for
these reasons, and as clients of a first-opinion farm animal practice connected with a
veterinary school, these farmers may not be representative of all UK dairy farms, and may
receive more veterinary visits to their farm or veterinary input due to the mutual benefit of
providing teaching opportunities for veterinary students. However, all the study farms were
commercial dairies and the information outlined in Table 1 demonstrates that these farms
represent herd sizes and management systems commonly found in the UK (24). As these data
are only presented from one veterinary practice the farms are located within a reasonably
limited geographic region. While this may have benefits in making the data from the farms
more comparable as all will have been influenced similarly by factors such as climate and
disease threats, it may mean that these farms are less representative of farms in other
locations which are subject to other influences.
Tables 1 and 2 demonstrate that a range of different systems and management practices are
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used across the seven study farms. These differences are likely to influence the initial, and
ongoing disease prevalence on the farms (e.g.: housing type is likely to affect lameness rates
and bedding type may influence mastitis rates). However, it is still possible for the aims of
the study to be achieved by analysing data from these various farms, demonstrating the
effects of the cessation of HP-CIAs on health and production parameters despite differing
initial levels or causative factors. This demonstrates that it may be possible to apply similar
prescribing changes to farms with a variety of management practices and expect to see health
and production parameters maintained, or improved, as they were on these study farms.
In this study, AMs prescribed to farms were assumed to represent AM use. It is possible that
some prescribed AMs may not have been administered to animals but may have gone unused
or been disposed of. For this reason, AM prescription is likely to overestimate use, however,
the authors judged this unlikely to be significant as each farm had weekly or bi-weekly
veterinary visits, making it unnecessary for AMs to be ‘stockpiled’.
Calculation of antimicrobial use
The comparison of AM prescribing using two metrics (Tables 3 and 4) highlights the degree
of change implemented by VSs and farmers; HP-CIAs represent a small proportion of the
quantity (kg) of AMs used in 2010-12 but represent a far larger proportion of ADD
administered in the same years. This is particularly true of the use of HP-CIAs in
intramammary tubes. The way in which the ADD metric is reported alongside kg of AMs
prescribed demonstrates the ways in which different analyses of AM use can represent these
data differently, as has been described by Mills and colleagues (25). Calculation of mean AM
consumption in mg/kg values (as calculated by mg/PCU) for each year of the study was
included to demonstrate the AM prescription of these herds in comparison with the 50 mg/kg
target suggested by the O’Neill Report (1) and adopted for the UK across the combined
livestock sectors (26), as well as the Responsible Use of Medicines in Agriculture Alliance
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(RUMA) Targets Task Force report dairy sector targets of a 50% reduction in use of HP-
CIAs between 2015 and 2020 and a total usage target of 21mg/PCU by 2020 (27). It should
be noted that a move away from HP-CIAs towards other AM treatments is likely to initially
increase the total mg/kg (or mg/PCU) use due to differences in dose rates. However, if
combined with effective changes in herd health management which reduce overall disease
incidence, this need not be a long-term effect. Conversely driving down total mg/kg targets
could have unintended consequences if veterinary surgeons were to increase their reliance on
low dose HP-CIAs.
Antimicrobial prescription
Similar to other studies (28-30), penicillins and 1st generation cephalosporins were
prescribed in the highest quantity (kg) in 2014 and 2015. Tetracyclines were also commonly
prescribed, as has been previously reported (28, 30). Antimicrobial use by the farms in this
study differs from that of farms in similar studies (28, 29), in which 3rd and 4th generation
cephalosporins were among the most frequently used AM classes). These findings suggest
that the groups of AMs used most frequently by farms in this study (penicillins, 1st generation
cephalosporins and tetracyclines) are also commonly used on other dairy farms in other
developed dairy areas of the world, and, as has been found by other authors, the reduced use
of HP-CIAs results in a shift towards the use of penicillins and broad-spectrum AMs (31).
The mean AM prescription to these farms across all years (range 12 – 18 mg/kg) was similar
to the median and mean AM use on British dairy farms in another recent UK study (32).
After prescribing changes were implemented on farms during 2011-12, the total quantities of
AMs prescribed in kg increased by 52% (Table 4). This was in part due to the differences in
mgs/dose of first line antimicrobials and HP-CIAs resulting in the total use of AMs appearing
falsely elevated, demonstrated by a smaller increase (25%) as represented by ADD. However,
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across both metrics, the quantities of AMs prescribed during 2012 and 2013 were higher than
in 2011, suggesting increased use to treat disease in these years.
Health and production parameters
Milk yield on these farms remained stable over the study period, demonstrating that
production was maintained alongside a cessation of HP-CIA use and an overall decrease in
ADD prescribed through 2014-15 (Figure 3).
Prior to prescription policy changes made in 2011-2012, farmers would frequently treat cows
that were systemically unwell due to retained foetal membranes or metritis with injectable 3rd
generation cephalosporins. Subsequent to prescription policy changes, cattle with these
diseases were treated with aminopenicillin preparations or amoxicillin-clavulanic acid
combinations. It is assumed that a significant deterioration in uterine health would have
negative impacts on fertility parameters (34, 35), however no negative effects on fertility
parameters were observed in association with the reduction in HP-CIAs on these farms; in
fact, the calving index decreased, the 100-day in-calf rate increased and mean number of days
from calving to conception showed a decreasing trend through 2010-15 (Figure 4).
The protocol for the antibiotic treatment of endometritis (intrauterine 1st generation
cephalosporin licenced for this purpose in cattle) did not change on any of the farms
throughout the study period. It is therefore unsurprising that the mean failure to cure rate of
endometritis remained stable.
Mean clinical mastitis case rates are reported for reference (Figure 5A), and it should be
noted that they are lower than the average clinical mastitis case rates on farms in England and
Wales (estimated to be 47 cases/100 cows/year (equating to a case rate of 0.47) (36)). The
increase in clinical mastitis case rate in 2012/13 corresponds to the increase in prescription of
AMs during these years and so is likely to contribute to the increased AM use in these years.
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Despite variation in clinical mastitis case rates throughout the six study years, the clinical
mastitis cure rates improved, suggesting that the treatments being used through 2014 and
2015 (none of which contained HP-CIAs) appeared to be at least as effective at achieving a
cure as the AMs being used in 2010, when 40% of ADD of intramammary preparations
prescribed contained HP-CIAs. This is consistent with a study in which implementation of a
restricted AM usage policy in Dutch herds did not impact negatively on udder health (37).
HP-CIAs were not used in dry cow treatments in 2010; dry cow treatment protocols were
therefore not changed between 2010 and 2015. The trend towards lower dry cow cure rates
may be due to changes in mastitis pathogens, changes in dry cow management or in
decreased efficacy of dry cow intramammary treatments, but it is difficult to differentiate
between these with the data available.
Prior to prescription policy changes, infectious causes of lameness in milking cows (in
particular interdigital necrobacillosis) would commonly have been treated with injectable 3rd
generation cephalosporin preparations. Although primarily affected by management factors,
lameness rates would be expected to have increased if infectious causes of lameness had a
poor treatment recovery rate. The fact that mobility scores from all six farms for which there
are data available shows a general reduction in the rates of lameness at mobility scores
indicates that foot health can also be maintained alongside reduced HP-CIA use, specifically
through the use of 1st generation cephalosporins and aminopenicillins in place of 3rd
generation cephalosporins.
It is possible that animal health may have been deteriorating without altering the health
parameters assessed if culling rates on the farms had increased significantly. Maximum
culling rates through 2013-15, however, were lower than those of 2010-12, while the
minimum culling rate remained at a similar level. Mean percentage change and associated
CIs suggest that culling rates were maintained through all six years of the study (Figure 7).
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As this was a retrospective study, only health data and production parameters that were
available from milk recording data and on-farm records could be analysed. Rather than assess
the efficacy of specific treatment changes for particular diseases, this study sought to provide
evidence about the effects on production and welfare parameters of reducing HP-CIAs on
dairy farms. Where possible, individual animal treatment outcomes were assessed and
presented. Although many treatment outcomes may be of interest (including outcomes of
pneumonia treatments in calves, clinical cure rates of pneumonia in calves or cases of
interdigital necrobacillosis in dairy cows), not all of these could be assessed due to
insufficient or inappropriate on-farm records.
Future work in this area should consider prospective evaluations of individual animal
treatment outcomes for specific diseases over time as AM use changes, with consistent
follow-up of cases and recording of clinical or bacteriological cures.
Changing prescribing practice
While HP-CIAs were used on all seven farms at the beginning of the study period, some
farms had higher use than others, and the time taken to implement strategies to reduce HP-
CIA use also varied between farms. This may reflect, in part, both the farmers’ willingness to
change AM use and individual VS’s willingness to alter on-farm treatment protocols or their
own prescribing practice. The increasing uptake of prescribing changes through the study
period may also reflect both farmers’ and VSs’ perception of responsible AM use which may
have been influenced by increasing public, political and industry pressures regarding AM use
in agriculture during this time. Within two years of practice-wide implementation of
prescribing changes, however, all six of the seven study farms that were clients of the FAP at
the start of the study period had either significantly reduced or altogether ceased use of HP-
CIAs. While changes on the majority of farms occurred over a period of time (one to two
years), the farm that joined the practice at the end of 2013 (Farm 6) changed its use of HP-
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CIAs with immediate effect after joining the practice and initiated use of SDCT, providing
evidence that prescribing changes can be enacted quickly on farms. The changes to
prescribing practice demonstrated in this study were made alongside various strategies to
improve animal management and husbandry on the farms which subsequently resulted in a
net decrease in doses (ADD) of AMs being prescribed, despite an increase in the use of
certain AM classes. Through the results of this study we propose that reducing the need to
prescribe AMs by working to improve herd health, rather than forcibly avoiding the
prescription or use of AMs, offers a sustainable way to safeguard animal health and welfare
and maintain food production alongside reduced AM use. It should also be considered that
reducing AM use through the process of improved herd health has many more economic
advantages for the farm than purely changing or reducing AM use.
A cessation of the use of HP-CIAs and a decrease in the use of AMs within the livestock
industry should be a key target for farmers and VSs and has been shown to be achievable
whilst maintaining animal health, welfare and production.
Data and analyses of the sort presented here are crucial to addressing barriers that farmers
and VSs face when deciding to alter their AM use and provide much-needed evidence to aid a
shift in the ‘social norm’ of AM use in production animal medicine.
Conclusions
This is the first study to demonstrate that dairy cattle health and welfare - as measured by
culling rates, production parameters, fertility, udder health and mobility data - can be
maintained, if not improved, alongside a complete cessation in the use of HP-CIAs as well as
an overall reduction of AM use on dairy farms when prescribing practices are altered in line
with proactive herd health planning strategies.
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Acknowledgements
The authors wish to thank the VSs and clients of Langford FAP for their assistance in
collecting and allowing access to their farm data. Thanks also to the members of the
University of Bristol’s Farm Animal Group for their input and advice, and to the Pat Impson
Memorial Fund and Langford Trust for supporting the work via their sponsorship of the Pat
Impson Residency in Bovine Health Management.
References
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14. Department of Health. UK Five Year Antimicrobial Resistance Strategy 2013 to 2018. In: health Do, editor. London2013. 15. Speksnijder DC, Jaarsma DAC, Verheij TJM, Wagenaar JA. Attitudes and perceptions of Dutch veterinarians on their role in the reduction of antimicrobial use in farm animals. Preventive Veterinary Medicine. 2015;121(3/4):365-73. 16. Coyne LA, Pinchbeck GL, Williams NJ, Smith RF, Dawson S, Pearson RB, et al. Understanding antimicrobial use and prescribing behaviours by pig veterinary surgeons and farmers: a qualitative study. Veterinary Record. 2014;175(23):593-. 17. Speksnijder DC, Jaarsma ADC, van der Gugten AC, Verheij TJM, Wagenaar JA. Determinants Associated with Veterinary Antimicrobial Prescribing in Farm Animals in the Netherlands: A Qualitative Study. Zoonoses and Public Health. 2015;62:39-51. 18. Vaarst M, Thamsborg SM, Bennedsgaard TW, Houe H, Enevoldsen C, Aarestrup FM, et al. Organic dairy farmers' decision making in the first 2 years after conversion in relation to mastitis treatments. Livestock Production Science. 2003;80(1-2):109-20. 19. Critically Important antibiotics in veterinary medicine: European medicines agency recommendations [press release]. https://www.noah.co.uk/wp-content/uploads/2016/12/NOAH-briefing-on-CIAs-07122016.pdf2016. 20. Allience RRuoMiA. RUMA adopts Europeam Medicines Agency 'highest priority' antibiotics list 2017 [Available from: http://www.ruma.org.uk/ruma-adopts-european-medicines-agency-highest-priority-antibiotics-list/. 21. Hadfield JD. MCMC methods for
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34. LeBlanc SJ, Duffield TF, Leslie KE, Bateman KG, Keefe GP, Walton JS, et al. Defining and diagnosing postpartum clinical endometritis and its impact on reproductive performance in dairy cows. Journal of Dairy Science. 2002;85(9):2223-36. 35. Gobikrushanth M, Salehi R, Ambrose DJ, Colazo MG. Categorization of endometritis and its association with ovarian follicular growth and ovulation, reproductive performance, dry matter intake, and milk yield in dairy cattle. Theriogenology. 2016;86(7):1842-9. 36. Bradley AJ, Leach KA, Breen JE, Green LE, Green MJ. Survey of the incidence and aetiology of mastitis on dairy farms in England and Wales. Veterinary Record. 2007;160(8):253-8. 37. Santman-Berends I, Swinkels JM, Lam T, Keurentjes J, van Schaik G. Evaluation of udder health parameters and risk factors for clinical mastitis in Dutch dairy herds in the context of a restricted antimicrobial usage policy. Journal of Dairy Science. 2016;99(4):2930-9.
Tables
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Table 1. Herd information and management practices for seven dairy farms in South West England 1
Farm No. of cows
(2010)
No. of cows
(2015)
Avg 305d yield - litres
(2015)
Breed of cows
Animals bought in Housed vs. grazing Bedding
Selective
dry cow
therapy²
(2010)
Selective
dry cow
therapy²
(2015)
Slurry stored in
a pit
1 147 123 6163 British
Friesian Bulls only
Graze through
summer Straw No No No
2 195 209 8475 Holstein X¹ Bulls only Graze through
summer Deep sawdust Yes Yes Yes
3 198 177 9628 Holstein Milking heifers Housed all year Sand topped rubber
mattresses Yes Yes Yes
4
159 174 10226 Holstein Bulls only Graze through
summer Sawdust topped rubber mats Yes Yes
Yes
5 166 195 8696 Holstein X¹ Bulls only Graze through
summer Deep sand Yes Yes Yes
6 180 143 9433 Holstein Milking cows & heifers Housed all year Sawdust topped rubber
mattresses No Yes Yes
7 131 219 10709 Holstein In-calf heifers and milking
heifers Housed all year Deep sand Yes Yes Yes
2
¹ The majority of animals in this herd are crossbred Holsteins. Breeds crossed with Holsteins are primarily Swedish Red, Jersey, Danish Red, Montbeliarde and Fleckvieh. 3 4 ²Biggs et al., 2016 5 6
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Table 2. Assessment of whether reliable or accessible on-farm recorded data were available for collection and analysis from each of seven dairy farms 7
Farm Services Observed
heats Clinical mastitis
Lameness treatments
Dry off dates Pregnancy diagnosis
results Endo- metritis Metritis
Mobility scores
1 Yes No Yes Yes Yes Yes Yes Yes Yes
2 Yes Yes Yes Yes Yes Yes Yes Yes Yes
3 Yes Yes Yes Yes Yes Yes Yes Yes Yes
4 Yes Yes Yes No Yes Yes Yes Yes Yes
5 Yes No No No Yes Yes No No Yes
6 Yes Yes Yes Yes Yes Yes Yes Yes No
7 Yes Yes Yes Yes Yes Yes Yes Yes Yes
8
9
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Table 3: Licenced routes of administration of antimicrobials prescribed to seven study farms each year from 2010 to 2015 calculated as total kilograms (kg) and animal 10 daily doses (ADDs). Antimicrobials are classed as first line or highest priority critically important antimicrobials (HP-CIAs); intramammary tubes are split by lactating cow 11 (LC) and dry cow (DC) treatments. 12
2010 2011 2012 2013 2014 2015
kg ADD kg ADD kg ADD kg ADD kg ADD kg ADD
Systemic 1st line 10.8 6.5 8.3 7.0 13.4 17.1 15.4 21.1 13.1 11.7 11.3 9.7
Systemic HP-CIAs
0.7 4.4 0.1 4.1 0.4 2.0 0.1 1.1 0.0 0.1 0.0 0.0
Intramammary LC 1st line
0.4 2.2 0.6 2.1 0.8 4.0 0.7 3.4 1.1 4.5 0.8 4.8
Intramammary LC HP-CIAs
0.2 2.8 0.2 3.0 0.1 1.1 0.0 0.3 0.0 0.0 0.0 0.0
Intramammary DC 1st line
0.9 1.5 0.9 1.7 0.9 1.1 0.9 1.1 0.9 1.0 1.1 1.5
Topical 1st line 0.0 0.1 0.0 0.1 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.2
Intrauterine 1st line
0.1 0.6 0.1 0.3 0.0 0.8 0.0 0.3 0.0 0.6 0.0 0.6
TOTAL 13.0 18.1 10.2 18.3 15.5 26.1 17.1 27.4 15.1 17.9 13.2 16.7
13
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Table 4: Classes of antimicrobials prescribed to seven study farms in 2010 – 2015, in kilograms (kg) and animal daily doses (ADDs) 14
2010 2011 2012 2013 2014 2015
kg ADD kg ADD kg ADD kg ADD kg ADD kg ADD
3rd generation cephalosporins
0.5 3.3 0.4 3.2 0.2 1.5 0.1 1.0 0.0 0.1 0.0 0.0
4th generation cephalosporins
0.2 3.8 0.2 3.9 0.1 2.1 0.0 0.5 0.0 0.0 0.0 0.0
Fluroquinolones 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0
Penicillins 4.2 4.8 4.0 5.0 6.3 7.3 7.2 7.1 5.8 5.2 5.5 5.0
Amoxicillins with clavulanic acid
0.0 0.9 0.0 0.6 0.3 7.4 0.4 9.5 0.3 6.1 0.4 6.2
1st generation cephalosporins
0.5 1.5 0.3 1.2 1.6 2.3 1.4 2.2 2.1 3.0 1.6 2.3
Potentiated sulphonamides
0.2 1.6 0.4 1.0 0.5 0.7 1.3 1.2 1.1 0.9 0.5 1.2
Macrolides 0.0 0.2 0.0 0.4 0.1 0.6 0.0 1.2 0.1 0.5 0.0 0.2
Lincosamides 0.0 0.0 0.0 0.0 0.0 0.2 0.0 0.0 0.0 0.1 0.0 0.0
Chloramphenicol derivatives
0.9 0.0 0.5 0.0 0.4 0.0 0.5 0.0 0.2 0.0 0.1 0.0
Aminoglycosides 4.2 0.2 2.8 0.1 4.6 0.1 4.1 0.1 3.5 0.0 3.3 0.0
Aminocoumarins 0.1 0.2 0.1 1.8 0.2 3.4 0.2 3.2 0.2 1.1 0.1 0.6
Tetracyclines 2.2 1.6 1.5 1.0 1.2 0.7 1.9 1.2 1.8 0.9 1.8 1.2
TOTAL 13.0 18.1 10.2 18.3 15.5 26.1 17.1 27.4 15.1 17.9 13.2 16.7
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Figure legends: 15
Table 1. Herd information and management practices for seven dairy farms in South West England 16
Table 2. Table demonstrating whether reliable or accessible on-farm recorded data was available for collection and analysis from each of the seven dairy 17
farms in the study. 18
Figure 2: Use of critically important antimicrobials used across all seven study farms, in kgs, by year. Farm 6 joined Langford Farm Animal Practice at the end 19
of 2013. 20
Table 3: Table showing the licenced routes of administration of antimicrobials prescribed to the seven study farms each year from 2010 to 2015 calculated 21
by kilograms (kgs) and animal daily doses (ADDs). Antimicrobials are classed as first line or critically important antimicrobials (CIAs), intramammary tubes 22
are also split by Lactating cow (LC) and Dry cow (DC) treatments. 23
Table 4: Classes of antimicrobials prescribed to the seven study farms in 2010 – 2015, in kilograms (kgs) and animal daily doses (ADDs) 24
Figure 3: Average 305-day milk yield for each of the seven farms during each year of the study (coloured lines). Geometric mean 305-day yield from all 25
seven farms (grey central line) and associated credible intervals (CI; upper and lower grey lines). Mean increase = 0.6%, CI = -0.2, 1.4. 26
Figure 4: A) 100-day in calf rate B) Calving index and for each of seven farms across six years. The grey areas show the variation in the inferred slope of the 27
mean (M, central grey line) with the intercept on the y-axis being the geometric-mean value across the seven farms in 2010. The top and bottom grey lines 28
represent the upper and lower 95% credible intervals (CI), respectively. 100-day in calf rate; M=5.0%; 95% CI 1.8, 7.8, Calving index; M= -0.9 %, 95% CI -1.4, -29
0.5.. 30
Figure 5: A) Clinical mastitis case rate per 100 cows per year on six farms over six years. B) Clinical mastitis all case cure rate per 100 cows per year for six 31
farms over six years. (n.b. Farm 5 is not represented as on-farm clinical mastitis records were not complete). The grey areas show the variation in the 32
inferred slope (M, central black lines) with the intercept on the y-axis being the geometric-mean value across the seven farms in 2010. The top and bottom 33
grey lines represent the upper and lower 95% credible intervals (CI), respectively. Clinical mastitis case rate; M=-7.8%, 95% CI -16.1, 0.1. Mean mastitis cure 34
rates; M=7.5% ,95% CI 1.2, 13.3. 35
Figure 6: Average bulk milk tank somatic cell count (BMTSCC) for each of the seven farms during each year of the study (coloured lines). Geometric mean 36
BMTSCC from all seven farms (M, grey central line) and associated credible intervals (CI) (upper and lower grey lines). BTMSCC; M= - 1.4, 95% CI -9.4, 5.9. 37
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Figure 7: Percentage of cows scored lame at mobility scoring performed on six farms by veterinarians between 2010 and 2015. Y-axis shows the percentage 38
of cows affected. (n.b. Farm 6 is not represented as mobility scoring records were not complete). The grey areas show the variation in the inferred slope (M, 39
central black lines) with the intercept on the y-axis being the geometric-mean value across the seven farms in 2010. The top and bottom black lines 40
represent the upper and lower 95% credible intervals (CI), respectively. Lameness rate; M = -18.2, 95% CI -24.1, -12.5. 41
Figure 8: Number of cows culled each year as a percentage of the number of cows in the milking herd for seven farms across six years. Y-axis shows the % of 42
cows culled each year. The grey area shows the variation in the inferred slope (M, central grey line) with the intercept on the y-axis being the geometric-43
mean value across the seven farms in 2010. The top and bottom grey lines represent the upper and lower 95% credible intervals (CI), respectively. Cull rate 44
M = -3.7, 95% CI -8.1, 0.6. 45
46